Emerging Tick-Borne Infections in Mainland China: an Increasing Public Health Threat
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View metadata, citation and similar papers at core.ac.uk brought to you by CORE HHS Public Access provided by IUPUIScholarWorks Author manuscript Author ManuscriptAuthor Manuscript Author Lancet Infect Manuscript Author Dis. Author Manuscript Author manuscript; available in PMC 2016 May 18. Published in final edited form as: Lancet Infect Dis. 2015 December ; 15(12): 1467–1479. doi:10.1016/S1473-3099(15)00177-2. Emerging tick-borne infections in mainland China: an increasing public health threat Li-Qun Fang#, Kun Liu#, Xin-Lou Li, Song Liang, Yang Yang, Hong-Wu Yao, Ruo-Xi Sun, Ye Sun, Wan-Jun Chen, Shu-Qing Zuo, Mai-Juan Ma, Hao Li, Jia-Fu Jiang, Wei Liu, X Frank Yang, Gregory C Gray, Peter J Krause, and Wu-Chun Cao State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, China (L-Q Fang PhD, K Liu MS, X-L Li MS, H-W Yao MS, R-X Sun BS, Y Sun BS, W-J Chen BS, S-Q Zuo PhD, M-J Ma PhD, H Li PhD, J-F Jiang PhD, Prof W Liu PhD, Prof W-C Cao PhD); College of Public Health and Health Professions, and Emerging Pathogens Institute, University of Florida, Gainesville, FL, USA (S Liang PhD, Y Yang PhD); Department of Microbiology and Immunology, Indiana University School of Medicine, Barnhill, IN, USA (Prof X F Yang PhD); Duke University School of Medicine, Durham, NC, USA (Prof G C Gray MD); and Department of Epidemiology of Microbial Diseases, Yale School of Public Health, and Department of Medicine and Department of Pediatrics, Yale School of Medicine, New Haven, CT, USA (P J Krause MD) # These authors contributed equally to this work. Abstract Since the beginning of the 1980s, 33 emerging tick-borne agents have been identified in mainland China, including eight species of spotted fever group rickettsiae, seven species in the family Anaplasmataceae, six genospecies in the complex Borrelia burgdorferi sensu lato, 11 species of Babesia, and the virus causing severe fever with thrombocytopenia syndrome. In this Review we have mapped the geographical distributions of human cases of infection. 15 of the 33 emerging tick-borne agents have been reported to cause human disease, and their clinical characteristics have been described. The non-specific clinical manifestations caused by tick-borne pathogens present a major diagnostic challenge and most physicians are unfamiliar with the many tick-borne diseases that present with non-specific symptoms in the early stages of the illness. Advances in and application of modern molecular techniques should help with identification of emerging tick- borne pathogens and improve laboratory diagnosis of human infections. We expect that more novel tick-borne infections in ticks and animals will be identified and additional emerging tick- borne diseases in human beings will be discovered. Correspondence to: Prof Wu-Chun Cao, State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Fengtai District, Beijing 100071, China [email protected]. Contributors L-QF, SL, XFY, GCG, PJK, and W-CC initiated the original ideas for the review. KL, X-LL, H-WY, RXS, YS, and W-JC contributed to the literature search and extracted data. KL, X-LL, H-WY, YY, SL, S-QZ, M-JM, HL, J-FJ, and WL assessed the data. L-QF, KL, X-LL, H-WY, R-XS, YS, W-JC, and W-CC created the figures. L-QF, GCG, and W-CC wrote the draft, and all authors contributed to the review and revision of the paper. Declaration of interests We declare no competing interests. Fang et al. Page 2 Author ManuscriptAuthor Introduction Manuscript Author Manuscript Author Manuscript Author Ticks were the first arthropods to be recognised as vectors that can transmit pathogens to human beings and are second only to mosquitoes as vectors of infectious diseases in the world.1 Tick-borne infections are zoonoses with pathogens maintained in natural cycles involving tick vectors and animal hosts. Human beings are occasional hosts for ticks and are usually viewed as dead-end hosts that have no role in maintaining tick-borne agents in nature.2 Different tick species favour distinct biotopes or environments, which define their geographical distribution and, consequently, the areas of risk for human tick-borne infections. In the past three decades, tick-borne pathogens have emerged worldwide and become a great threat to human health.1,3 China is the largest developing country in the world and has made tremendous progress in the control and prevention of infectious diseases; however, emerging infectious diseases are the new challenge now facing China.4 Although outbreaks of severe acute respiratory syndrome and H5N1 and H7N9 avian influenza virus infections have attracted great attention, emerging tick-borne diseases have generally been neglected by primary health- care providers and clinicians. Although an increasing number of tick-borne infections have been reported in mainland China, no comprehensive review of this substantial public health problem has been undertaken. We will provide an overview of the type and distribution of emerging tick-borne infections in tick vectors, animal hosts, and human beings. We will describe the clinical characteristics of human tick-borne diseases, and discuss possible factors contributing to their emergence. Emergence of tick-borne infections in mainland China Since 1982, 33 emerging tick-associated agents have been identified in mainland China, including eight species of spotted fever group rickettsiae (SFGR);5–11 three species of Ehrlichia,12–14 three species of Anaplasma,15–17 and Candidatus Neoehrlichia mikurensis18 in the family Anaplasmataceae; six genospecies in the complex Borrelia burgdorferi sensu lato;19–23 11 species of Babesia;24–33 and severe fever with thrombocytopenia syndrome virus (SFTSV).34 The location and year in which each emerging tick-borne agent was first identified are shown in the appendix. Most (19 of 33) were initially detected in ticks; however, six were identified in domestic animals (sheep, goat, buffalo, and dog), two in wild animals (Chinese white-bellied rat and Chinese hare), and six in people. Detailed information regarding the identification of these emerging tick-borne infections is summarised in table 1. Among the 33 newly recognised tick-associated agents, 15 have been reported to cause human infection, including: four species of SFGR;11,35,46,48 an Ehrlichia species,53 two Anaplasma species,17,53 and Candidatus N mikurensis;18 three genospecies of B burgdorferi sensu lato;19,21,78 three species of Babesia;33,104,108 and SFTSV (table 2).34 Six of the tick- borne pathogens were first identified in febrile patients (Candidatus Rickettsia tarasevichiae, Candidatus N mikurensis, Borrelia garinii, Borrelia afzelii, Babesia venatorum [not yet formally described], and SFTSV) and then shown to be associated with ticks (table 1). The other nine human pathogens were initially detected in ticks or animals and subsequently Lancet Infect Dis. Author manuscript; available in PMC 2016 May 18. Fang et al. Page 3 shown to infect human beings (Rickettsia heilongjiangiensis, Rickettsia sibirica sp BJ-90, Author ManuscriptAuthor Manuscript Author Manuscript Author Manuscript Author Rickettsia raoultii, Ehrlichia chaffeensis, Anaplasma phagocytophilum, Anaplasma capra, Borrelia valaisiana-related genospecies, Babesia microti, and Babesia divergens). Among these 15 emerging tick-borne diseases, severe fever with thrombocytopenia syndrome (SFTS) was first identified in mainland China34 and subsequently reported in South Korea and Japan.134,135 A disease similar to SFTS has been reported in the USA.136 Human infections with R sibirica sp BJ-90, Candidatus R tarasevichiae, A capra, and B valaisiana- related genospecies have been exclusively diagnosed in mainland China.11,17,46,78 Human infections of Candidatus N mikurensis, Ba venatorum, and R raoultii, which have been detected in China, were first identified in Europe.18,33,48 Five tick-borne pathogens have been detected in ticks or reservoir hosts, or both, but have not yet been reported to cause infection in human beings in China. They include Rickettsia monacensis, Rickettsia slovaca, Rickettsia sibirica sp mongolotimonae, B valaisiana, and B burgdorferi sensu stricto.137–141 Additionally, a Rickettsia species (Candidatus Rickettsia hebeiii), two Ehrlichia species (Ehrlichia canis and Ehrlichia sp Tibet), an Anaplasma species (Anaplasma platys), a genospecies of B burgdorferi sensu lato (Borrelia sinica), and eight Babesia species (Babesia ovis, Babesia ovata, Babesia orientalis, Babesia major, Babesia motasi, Babesia caballi, Babesia sp Kashi, and Babesia sp Xinjiang) have been identified in ticks or animals, but their pathogenicity to human beings is unknown. Emerging SFGR infections Eight novel species of SFGR have been recorded in mainland China since 1982 (table 1).5–11 These species are mainly distributed in northern China (north of 36° north latitude). Tick and animal infections The eight emerging species and uncharacterised species of SFGR have been shown to be associated with 16 tick species (figure 1). R heilongjiangiensis has been proven to infect a range of tick species, three rodent species, and goats (appendix). In northeastern China, R heilongjiangiensis was detected in nine tick species and two rodent species from Heilongjiang Province,36–38 and in Haemaphysalis spp ticks from Jilin Province.38 In Inner Mongolia, R heilongjiangiensis has been reported in Haemaphysalis verticalis, Detmacentor niveus, Hyalomma asiaticum kozlovi, Rhipicephalus pumilio, and Detmacentor